diff --git a/Lib/subprocess.py b/Lib/subprocess.py
index 4955f77b60381f..68d41462237924 100644
--- a/Lib/subprocess.py
+++ b/Lib/subprocess.py
@@ -2077,6 +2077,10 @@ def _communicate(self, input, endtime, orig_timeout):
                     self.stdin.flush()
                 except BrokenPipeError:
                     pass  # communicate() must ignore BrokenPipeError.
+                except ValueError:
+                    # ignore ValueError: I/O operation on closed file.
+                    if not self.stdin.closed:
+                        raise
                 if not input:
                     try:
                         self.stdin.close()
diff --git a/Lib/test/test_subprocess.py b/Lib/test/test_subprocess.py
index 9792d7c8983cd3..9275e444615af7 100644
--- a/Lib/test/test_subprocess.py
+++ b/Lib/test/test_subprocess.py
@@ -1062,6 +1062,19 @@ def test_writes_before_communicate(self):
         self.assertEqual(stdout, b"bananasplit")
         self.assertEqual(stderr, b"")
 
+    def test_communicate_stdin_closed_before_call(self):
+        # gh-70560, gh-74389: stdin.close() before communicate()
+        # should not raise ValueError from stdin.flush()
+        with subprocess.Popen([sys.executable, "-c",
+                               'import sys; sys.exit(0)'],
+                              stdin=subprocess.PIPE,
+                              stdout=subprocess.PIPE,
+                              stderr=subprocess.PIPE) as p:
+            p.stdin.close()  # Close stdin before communicate
+            # This should not raise ValueError
+            (stdout, stderr) = p.communicate()
+            self.assertEqual(p.returncode, 0)
+
     def test_universal_newlines_and_text(self):
         args = [
             sys.executable, "-c",
diff --git a/Misc/NEWS.d/next/Library/2025-11-29-04-20-44.gh-issue-74389.pW3URj.rst b/Misc/NEWS.d/next/Library/2025-11-29-04-20-44.gh-issue-74389.pW3URj.rst
new file mode 100644
index 00000000000000..a9bf5f80d80c9f
--- /dev/null
+++ b/Misc/NEWS.d/next/Library/2025-11-29-04-20-44.gh-issue-74389.pW3URj.rst
@@ -0,0 +1,3 @@
+When the stdin being used by a :class:`subprocess.Popen` instance is closed,
+this is now ignored in :meth:`subprocess.Popen.communicate` instead of
+leaving the class in an inconsistent state.